Pushing back: Wound mechanotransduction in repair and regeneration

Journal of Investigative Dermatology

Volumn 131, Issue 11, 2011, Pages 2186-2196

  Wong, Victor W ^a   Akaishi, Satoshi ^a   Longaker, Michael T ^a   Gurtner, Geoffrey C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN;

BIOMECHANICS; EXTRACELLULAR MATRIX; HOMEOSTASIS; HUMAN; KELOID; KERATINOCYTE; MECHANORECEPTOR; MECHANOTRANSDUCTION; NANOTECHNOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SKIN CELL; SKIN DISEASE; TISSUE REGENERATION; WOUND HEALING;

EID: 80054753943     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2011.212     Document Type: Review

References (126)

1. Aarabi S, Bhatt KA, Shi Y et al. (2007a) Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis. FASEB J 21: 3250-61 (Pubitemid 47565543)
2. Aarabi S, Longaker MT, Gurtner GC (2007b) Hypertrophic scar formation following burns and trauma: New approaches to treatment. PLoS Med 4:e234
3. Agache PG, Monneur C, Leveque JL et al. (1980) Mechanical properties and Young's modulus of human skin in vivo. Arch Dermatol Res 269:221-32 (Pubitemid 11207090)
4. Akaishi S, Akimoto M, Hyakusoku H et al. (2010) The tensile reduction effects of silicone gel sheeting. Plast Reconstr Surg 126:109e-11e
5. Akaishi S, Akimoto M, Ogawa R et al. (2008a) The relationship between keloid growth pattern and stretching tension: Visual analysis using the finite element method. Ann Plast Surg 60:445-51 (Pubitemid 351440816)
6. Akaishi S, Ogawa R, Hyakusoku H (2008b) Keloid and hypertrophic scar: Neurogenic inflammation hypotheses. Med Hypotheses 71:32-8
7. Alenghat FJ, Ingber DE (2002) Mechanotransduction: All signals point to cytoskeleton, matrix, and integrins. Sci STKE 2002:PE6
8. Alster TS, Tanzi EL (2003) Hypertrophic scars and keloids: Etiology and management. Am J Clin Derm 4:235-43 (Pubitemid 36506429)
9. Atkinson JA, McKenna KT, Barnett AG et al. (2005) A randomized, controlled trial to determine the efficacy of paper tape in preventing hypertrophic scar formation in surgical incisions that traverse Langer's skin tension lines. Plast Reconstr Surg 116:1648-56; discussion 57-58 (Pubitemid 41608332)
10. Baneyx G, Baugh L, Vogel V (2002) Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc Natl Acad Sci USA 99:5139-43 (Pubitemid 34411516)
11. Blanpain C, Fuchs E (2009) Epidermal homeostasis: A balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 10:207-17
12. Borgquist O, Ingemansson R, Malmsjo M (2010) Wound edge microvascular blood flow during negative-pressure wound therapy: Examining the effects of pressures from -10 to -175 mmHg. Plast Reconstr Surg 125:502-9
13. Bornstein P, Sage EH (2002) Matricellular proteins: Extracellular modulators of cell function. Curr Opin Cell Biol 14:608-16 (Pubitemid 35247745)
14. Butler PD, Longaker MT, Yang GP (2008) Current progress in keloid research and treatment. J Am Coll Surg 206:731-41
15. Carruthers J, Fagien S, Matarasso SL (2004) Consensus recommendations on the use of botulinum toxin type a in facial aesthetics. Plast Reconstr Surg 114:1S-22S (Pubitemid 40354480)
16. Chaqour B, Goppelt-Struebe M (2006) Mechanical regulation of the Cyr61/ CCN1 and CTGF/CCN2 proteins. FEBS J 273:3639-49
17. Chin MSBA, Lancerotto LMD, Helm DLMD et al. (2009) Analysis of neuropeptides in stretched skin. Plast Reconstr Surg 124:102-13
18. Chiquet M, Tunc-Civelek V, Sarasa-Renedo A (2007) Gene regulation by mechanotransduction in fibroblasts. Appl Physiol Nutr Metab 32:967-73
19. Clark JA, Cheng JC, Leung KS (1996) Mechanical properties of normal skin and hypertrophic scars. Burns 22:443-6 (Pubitemid 26306105)
20. Cohen DM, Chen CS (2008) Mechanical control of stem cell differentiation. In: StemBook. (Bhatia S, Polak J, eds). Harvard Stem Cell Institute: Cambridge
21. Costa AM, Peyrol S, Porto LC et al. (1999) Mechanical forces induce scar remodeling. Study in non-pressure-treated versus pressure-treated hypertrophic scars. Am J Pathol 155:1671-9
22. Cuttle L, Kempf M, Phillips GE et al. (2006) A porcine deep dermal partial thickness burn model with hypertrophic scarring. Burns 32:806-20 (Pubitemid 44442605)
23. Dallon JC, Ehrlich HP (2008) A review of fibroblast-populated collagen lattices. Wound Repair Regen 16:472-9 (Pubitemid 352000311)
24. Daya M (2011) Abnormal scar modulation with the use of micropore tape. Eur J Plast Surg 34:45-51
25. Delanoe-Ayari H, Rieu JP, Sano M (2010) 4D traction force microscopy reveals asymmetric cortical forces in migrating Dictyostelium cells. Phys Rev Lett 105:248103
26. Derderian CA, Bastidas N, Lerman OZ et al. (2005) Mechanical strain alters gene expression in an in vitro model of hypertrophic scarring. Ann Plast Surg 55:69-75 (Pubitemid 40884801)
27. Discher DE, Janmey P, Wang Y-L (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139-43 (Pubitemid 41681732)
28. Distler JH, Jungel A, Caretto D et al. (2006) Monocyte chemoattractant protein 1 released from glycosaminoglycans mediates its profibrotic effects in systemic sclerosis via the release of interleukin-4 from T cells. Arthritis Rheum 54:214-25 (Pubitemid 43122204)
29. Distler JHW, Akhmetshina A, Schett G et al. (2009) Monocyte chemoattractant proteins in the pathogenesis of systemic sclerosis. Rheumatology 48:98-103
30. Dobrev H (1999a) Non-invasive monitoring of the mechanical properties of keloids during cryosurgery. Acta Derm Venereol 79:487-8
31. Dobrev HP (1999b) In vivo study of skin mechanical properties in patients with systemic sclerosis. J Am Acad Dermatol 40:436-42 (Pubitemid 29115305)
32. Dubin AE, Patapoutian A (2011) Nociceptors: The sensors of the pain pathway. J Clin Invest 120:3760-72
33. Dunn MG, Silver FH, Swann DA (1985) Mechanical analysis of hypertrophic scar tissue: Structural basis for apparent increased rigidity. J Invest Dermatol 84:9-13 (Pubitemid 15186215)
34. Eckes B, Krieg T (2004) Regulation of connective tissue homeostasis in the skin by mechanical forces. Clin Exp Rheumatol 22:S73-6 (Pubitemid 39162039)
35. Eckes B, Nischt R, Krieg T (2010) Cell-matrix interactions in dermal repair and scarring. Fibrogenesis Tissue Repair 3:4
36. Engler AJ, Sen S, Sweeney HL et al. (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677-89 (Pubitemid 44233625)
37. Escoffier C, de Rigal J, Rochefort A et al. (1989) Age-related mechanical properties of human skin: An in vivo study. J Invest Dermatol 93:353-7 (Pubitemid 19216071)
38. Estes BT, Gimble JM, Guilak F (2004) Mechanical signals as regulators of stem cell fate. Curr Top Dev Biol 60:91-126 (Pubitemid 39752360)
39. Expert Working Group (2008) Vacuum assisted closure: Recommendations for use. A consensus document. Int Wound J 5(Suppl 4) iii-19
40. Fuchs E, Horsley V (2008) More than one way to skin. Genes Dev 22: 976-85 (Pubitemid 351544236)
41. Ghahary A, Ghaffari A (2007) Role of keratinocyte-fibroblast cross-talk in development of hypertrophic scar. Wound Rep Regen 15 (Suppl 1):S46-53 (Pubitemid 47301674)
42. Gieni RS, Hendzel MJ (2008) Mechanotransduction from the ECM to the genome: Are the pieces now in place? J Cell Biochem 104:1964-87
43. Goldstein B, Sanders J (1998) Skin response to repetitive mechanical stress: A new experimental model in pig. Arch Phys Med Rehabil 79:265-72 (Pubitemid 28207113)
44. Guilak F, Cohen DM, Estes BT et al. (2009) Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5:17-26
45. Gurtner GC, Dauskardt RH, Wong VW et al. (2011) Improving cutaneous scar by controlling the mechanical environment: Large animal and phase I studies. Ann Surg; e-pub ahead of print 19 May 2011
46. Gurtner GC, Werner S, Barrandon Y et al. (2008) Wound repair and regeneration. Nature 453:314-21 (Pubitemid 351693137)
47. Hadjipanayi E, Mudera V, Brown RA (2009a) Close dependence of fibroblast proliferation on collagen scaffold matrix stiffness. J Tissue Eng Regen Med 3:77-84
48. Hadjipanayi E, Mudera V, Brown RA (2009b) Guiding cell migration in 3D: A collagen matrix with graded directional stiffness. Cell Motil Cytoskeleton 66:121-8
49. Harris AK, Wild P, Stopak D (1980) Silicone rubber substrata: A new wrinkle in the study of cell locomotion. Science 208:177-9 (Pubitemid 10072133)
50. Harunari N, Zhu KQ, Armendariz RT et al. (2006) Histology of the thick scar on the female, red Duroc pig: Final similarities to human hypertrophic scar. Burns 32:669-77 (Pubitemid 44293069)
51. Harvey KA, Paranavitana CN, Zaloga GP et al. (2007) Diverse signaling pathways regulate fibroblast differentiation and transformation through Rho kinase activation. J Cell Physiol 211:353-63 (Pubitemid 46580089)
52. Hersen P, Ladoux B (2011) Biophysics: Push it, pull it. Nature 470:340-1
53. Hinz B, Phan SH, Thannickal VJ et al. (2007) The myofibroblast: One function, multiple origins. Am J Pathol 170:1807-16 (Pubitemid 47339255)
54. Hossain MM, Crish JF, Eckert RL et al. (2005) h2-Calponin is regulated by mechanical tension and modifies the function of actin cytoskeleton. J Biol Chem 280:42442-53
55. Huang S, Ingber DE (2005) Cell tension, matrix mechanics, and cancer development. Cancer Cell 8:175-6 (Pubitemid 41317587)
56. Hynes RO (2009) The extracellular matrix: Not just pretty fibrils. Science 326:1216-9
57. Ingber DE (2003a) Mechanobiology and diseases of mechanotransduction. Ann Med 35:564-77 (Pubitemid 38005314)
58. Ingber DE (2003b) Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci 116:1157-73 (Pubitemid 36410656)
59. Ingber DE (2003c) Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci 116:1397-408 (Pubitemid 36527487)
60. Ingber DE (2006) Cellular mechanotransduction: Putting all the pieces together again. FASEB J 20:811-27 (Pubitemid 44943939)
61. Ingber DE (2008) Tensegrity-based mechanosensing from macro to micro. Prog Biophys Mol Biol 97:163-79
62. Jaalouk DE, Lammerding J (2009) Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10:63-73
63. Jacobs S, Simhaee DA, Marsano A et al. (2009) Efficacy and mechanisms of vacuum-assisted closure (VAC) therapy in promoting wound healing: A rodent model. J Plast Reconstr Aesthet Surg 62:1331-8
64. Jakkaraju S, Zhe X, Pan D et al. (2005) TIPs are tension-responsive proteins involved in myogenic versus adipogenic differentiation. Dev Cell 9:39-49 (Pubitemid 40903658)
65. Jean C, Gravelle P, Fournie JJ et al. (2011) Influence of stress on extracellular matrix and integrin biology. Oncogene 30:2697-706
66. Jones DL, Wagers AJ (2008) No place like home: Anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 9:11-21
67. Karamichos D, Brown RA, Mudera V (2007) Collagen stiffness regulates cellular contraction and matrix remodeling gene expression. J Biomed Mater Res A 83:887-94 (Pubitemid 350086317)
68. Katsumi A, Orr AW, Tzima E et al. (2004) Integrins in mechanotransduction. J Biol Chem 279:12001-4 (Pubitemid 38445760)
69. Kessler-Becker D, Krieg T, Eckes B (2004) Expression of pro-inflammatory markers by human dermal fibroblasts in a three-dimensional culture model is mediated by an autocrine interleukin-1 loop. Biochem J 379:351-8 (Pubitemid 38570108)
70. Khatyr F, Imberdis C, Vescovo P et al. (2004) Model of the viscoelastic behaviour of skin in vivo and study of anisotropy. Skin Res Technol 10:96-103 (Pubitemid 38559510)
71. Knies Y, Bernd A, Kaufmann R et al. (2006) Mechanical stretch induces clustering of beta1-integrins and facilitates adhesion. Exp Dermatol 15:347-55 (Pubitemid 44056481)
72. Kose O, Waseem A (2008) Keloids and hypertrophic scars: Are they two different sides of the same coin? Derm Surg 34:336-46
73. Krammer A, Lu H, Isralewitz B et al. (1999) Forced unfolding of the fibronectin type III module reveals a tensile molecular recognition switch. Proc Natl Acad Sci USA 96:1351-6
74. Langer K (1978) On the anatomy and physiology of the skin. I. The cleavability of the cutis (translated from Langer K (1861). Zur Anatomie und Physiologie der Haut. I. Uber die Spaltbarkeit der Cutis. Sitzungsbericht der Mathematisch-naturwissenschaftlichen Classe der Kaiserlichen Academie der Wissenschaften. 44: 19). Br J Plast Surg 31:3-8
75. Leask A, Abraham DJ (2006) All in the CCN family: Essential matricellular signaling modulators emerge from the bunker. J Cell Sci 119:4803-10 (Pubitemid 46017793)
76. Liu B, Kim TJ, Wang Y (2010) Live cell imaging of mechanotransduction. J R Soc Interface 7(Suppl 3):S365-75
77. Lorenz HP, Whitby DJ, Longaker MT et al. (1993) Fetal wound healing. The ontogeny of scar formation in the non-human primate. Ann Surg 217:391-6 (Pubitemid 23115343)
78. Lu F, Ogawa R, Nguyen DT et al. (2011) Microdeformation of threedimensional cultured fibroblasts induces gene expression and morphological changes. Ann Plast Surg 66:296-300
79. Lumpkin EA, Caterina MJ (2007) Mechanisms of sensory transduction in the skin. Nature 445:858-65
80. Malmsjo M, Ingemansson R, Martin R et al. (2009a) Negative-pressure wound therapy using gauze or open-cell polyurethane foam: Similar early effects on pressure transduction and tissue contraction in an experimental porcine wound model. Wound Repair Regen 17:200-5
81. Malmsjo M, Ingemansson R, Martin R et al. (2009b) Wound edge microvascular blood flow: Effects of negative pressure wound therapy using gauze or polyurethane foam. Ann Plast Surg 63:676-81
82. Matsui Y, Sadoshima J (2004) Rapid upregulation of CTGF in cardiac myocytes by hypertrophic stimuli: Implication for cardiac fibrosis and hypertrophy. J Mol Cell Cardiol 37:477-81 (Pubitemid 38953375)
83. Matthews BD, Overby DR, Mannix R et al. (2006) Cellular adaptation to mechanical stress: Role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119:508-18
84. Morykwas MJ, Argenta LC, Shelton-Brown EI et al. (1997) Vacuum-assisted closure: A new method for wound control and treatment: Animal studies and basic foundation. Ann Plast Surg 38:553-62 (Pubitemid 27251299)
85. Mustoe TA, Cooter RD, Gold MH et al. (2002) International clinical recommendations on scar management. Plast Reconstr Surg 110:560-71 (Pubitemid 34815962)
86. Ogawa R (2008) Keloid and hypertrophic scarring may result from a mechanoreceptor or mechanosensitive nociceptor disorder. Med Hypotheses 71:493-500
87. Orgill DP, Bayer LR (2011) Update on negative-pressure wound therapy. Plast Reconstr Surg 127(Suppl 1):105S-15S
88. Orgill DP, Manders EK, Sumpio BE et al. (2009) The mechanisms of action of vacuum assisted closure: More to learn. Surgery 146:40-51
89. Paszek MJ, Zahir N, Johnson KR et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241-54 (Pubitemid 41317594)
90. Ramos MLC, Gragnani A, Ferreira LM (2008) Is there an ideal animal model to study hypertrophic scarring? J Burn Care Res 29:363-8 (Pubitemid 351498833)
91. Reichelt J (2007) Mechanotransduction of keratinocytes in culture and in the epidermis. Eur J Cell Biol 86:807-16 (Pubitemid 350103020)
92. Runkel N, Krug E, Berg L et al. (2011) Evidence-based recommendations for the use of Negative Pressure Wound Therapy in traumatic wounds and reconstructive surgery: Steps towards an international consensus. Injury 42:Suppl 1:S1-12
93. Sanders JE, Mitchell SB, Wang YN et al. (2002) An explant model for the investigation of skin adaptation to mechanical stress. IEEE Trans Biomed Eng 49:1626-31 (Pubitemid 36055721)
94. Satish L, Kathju S (2010) Cellular and molecular characteristics of scarless versus fibrotic wound healing. Dermatol Res Pract 2010: 790234
95. Scherer SS, Pietramaggiori G, Mathews JC et al. (2009) Short periodic applications of the vacuum-assisted closure device cause an extended tissue response in the diabetic mouse model. Plast Reconstr Surg 124:1458-65
96. Sen S, Kumar S (2009) Combining mechanical and optical approaches to dissect cellular mechanobiology. J Biomech 43:45-54
97. Shrader CD, Ressetar HG, Luo J et al. (2008) Acute stretch promotes endothelial cell proliferation in wounded healing mouse skin. Arch Dermatol Res 300:495-504
98. Shynlova O, Tsui P, Dorogin A et al. (2008) Monocyte chemoattractant protein-1 (CCL-2) integrates mechanical and endocrine signals that mediate term and preterm labor. J Immunol 181:1470-9
99. Silver FH, Siperko LM, Seehra GP (2003) Mechanobiology of force transduction in dermal tissue. Skin Res Technol 9:3-23 (Pubitemid 36621682)
100. Solon J, Levental I, Sengupta K et al. (2007) Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93:4453-61 (Pubitemid 350294491)
101. Sun JH, Yang B, Donnelly DF et al. (2006) MCP-1 enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia. J Neurophysiol 96:2189-99 (Pubitemid 44785875)
102. Takei T, Kito H, Du W et al. (1998) Induction of interleukin (IL)-1 alpha and beta gene expression in human keratinocytes exposed to repetitive strain: Their role in strain-induced keratinocyte proliferation and morphological change. J Cell Biochem 69:95-103 (Pubitemid 28152943)
103. Tamaki K, Okochi H, Fujimoto M et al. (2004) Mechanical stretching in vitro regulates signal transduction pathways and cellular proliferation in human epidermal keratinocytes. J Invest Dermatol 122:783-90 (Pubitemid 38471349)
104. Torbrand C, Wackenfors A, Lindstedt S et al. (2008) Sympathetic and sensory nerve activation during negative pressure therapy of sternotomy wounds. Interact Cardiovasc Thorac Surg 7:1067-70
105. Tsunozaki M, Bautista DM (2009) Mammalian somatosensory mechanotransduction. Curr Opin Neurobiol 19:362-9
106. Venturi ML, Attinger CE, Mesbahi AN et al. (2005) Mechanisms and clinical applications of the vacuum-assisted closure (VAC) device: A review. Am J Clin Dermatol 6:185-94 (Pubitemid 40994261)
107. Vincent T, Saklatvala J (2006) Basic fibroblast growth factor: An extracellular mechanotransducer in articular cartilage? Biochem Soc Trans 34:456-7 (Pubitemid 43954011)
108. Wang JH, Lin JS (2007) Cell traction force and measurement methods. Biomech Model Mechanobiol 6:361-71 (Pubitemid 47551863)
109. Wang JH, Thampatty BP (2008) Mechanobiology of adult and stem cells. Int Rev Cell Mol Biol 271:301-46
110. Wang Y, Wang N (2009) FRET and mechanobiology. Integr Biol (Camb) 1:565-73
111. Wang Z, Fong KD, Phan TT et al. (2006) Increased transcriptional response to mechanical strain in keloid fibroblasts due to increased focal adhesion complex formation. J Cell Physiol 206:510-7 (Pubitemid 43062822)
112. Ward RS (1991) Pressure therapy for the control of hypertrophic scar formation after burn injury. A history and review. J Burn Care Rehabil 12:257-62
113. Webb K, Hitchcock RW, Smeal RM et al. (2006) Cyclic strain increases fibroblast proliferation, matrix accumulation, and elastic modulus of fibroblast-seeded polyurethane constructs. J Biomech 39:1136-44
114. Werner S, Krieg T, Smola H (2007) Keratinocyte-fibroblast interactions in wound healing. J Invest Dermatol 127:998-1008 (Pubitemid 46625161)
115. Wilhelmi BJ, Blackwell SJ, Phillips LG (1999) Langer's lines: To use or not to use. Plast Reconstr Surg 104:208-14 (Pubitemid 29283214)
116. Wilson AM (2006) Use of botulinum toxin type A to prevent widening of facial scars. Plast Reconstr Surg 117:1758-66; discussion 67-68 (Pubitemid 44324358)
117. Wolf CB, Mofrad MRK (2009) Mechanotransduction and its role in stem cell biology. In: Trends in Stem Cell Biology and Technology. (Bharavand H, ed) Humana Press: New York, 389-403
118. Wong VW, Sorkin M, Glotzbach JP et al. (2011) Surgical approaches to create murine models of human wound healing. J Biomed Biotechnol 2011:969618
119. Wray RC (1983) Force required for wound closure and scar appearance. Plast Reconstr Surg 72:380-2 (Pubitemid 13040074)
120. Wynn TA (2007) Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 117:524-9 (Pubitemid 46348506)
121. Xiao Z, Zhang F, Cui Z (2009) Treatment of hypertrophic scars with intralesional botulinum toxin type A injections: A preliminary report. Aesthetic Plast Surg 33:409-12
122. Xie Y, Zhu KQ, Deubner H et al. (2007) The microvasculature in cutaneous wound healing in the female red Duroc pig is similar to that in human hypertrophic scars and different from that in the female Yorkshire pig. J Burn Care Res 28:500-6 (Pubitemid 46733262)
123. Yagmur C, Akaishi S, Ogawa R et al. (2010) Mechanical receptor-related mechanisms in scar management: A review and hypothesis. Plast Reconstr Surg 126:426-34
124. Yang G, Crawford RC, Wang JH (2004) Proliferation and collagen production of human patellar tendon fibroblasts in response to cyclic uniaxial stretching in serum-free conditions. J Biomech 37:1543-50 (Pubitemid 39141847)
125. Zhang H, Landmann F, Zahreddine H et al. (2011) A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 471:99-103
126. Zhu Y, Luo J, Barker J et al. (2002) Identification of genes induced by rapid intraoperative tissue expansion in mouse skin. Arch Dermatol Res 293:560-8 (Pubitemid 34151127)